Gastropod species found in birds` nests from Argentina

Rev. Mus. Argentino Cienc. Nat., n.s.
17(1): 87-96, 2015
ISSN 1514-5158 (impresa)
ISSN 1853-0400 (en línea)
Gastropod species found in birds’ nests from Argentina
Sergio E. MIQUEL1, Paola TURIENZO² & Osvaldo R. DI IORIO²
¹ Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Av. Ángel Gallardo 470 (1405). Ciudad
Autónoma de Buenos Aires, República Argentina. e-mail: semsnail@yahoo.com.ar. ² Entomología.
Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad
de Buenos Aires. Ciudad Universitaria (C1428EHA) Ciudad Autónoma de Buenos Aires, República Argentina.
e-mails: paolaturienzo@yahoo.com; megacyllene@yahoo.com.ar
Abstract: Bird’s nests are specialized habitats that are inhabited by a diverse suite of invertebrates, such as
insects, spiders, pseudoscorpions, and ticks. This study presents a list of gastropods found in birds’ nests from
Argentina for the first time. A total of 138 specimens of gastropods, belonging to 11 species, 10 genera and 8
families of snails were present in the nests of 42 birds from 6 families in 6 provinces in Argentina. Fifty eight
specimens of the snail Pupisoma latens of different sizes were found alive in a nest, representing a new habitat
for this species, which has been previously described from the aerial parts of trees. The remaining species were
represented by dead specimens (fragments or empty shells), which can be tentatively attributed to bird diets.
Among these, the most abundant species were Bulimulus bonariensis bonariensis and Succinea meridionalis,
both as pre-adults. The nests Anumbius annumbi and Furnarius rufus from the province of Buenos Aires had the
highest number of specimens. Freshwater snails (Heleobia parchappii, Biomphalaria sp., and Drepanotrema sp.)
comprised 13% of the snail species found.
Key words: Mollusks, aquatic gastropods, landsnails, Pupisoma, birds, nest inhabitants, diet.
Resumen: Los nidos de aves son ejemplos de hábitats ocupados por un conjunto de invertebrados, como insectos, arañas, pseudoescorpiones, etc. Por primera vez se presenta una lista de gasterópodos encontrados en nidos
aviarios de la Argentina. Un total de 138 especímenes pertenecientes a 11 especies, 10 géneros y 8 familias fueron
hallados en 42 nidos de 6 familias de aves en 6 provincias. Sólo Pupisoma latens, representado por 58 especímenes de diferentes tamaños, fue encontrado vivo en un nido, siendo un nuevo hábitat de la especie, previamente
encontrada en partes aéreas de árboles. El resto de las especies estaban representadas por animales muertos
(fragmentos o conchillas vacías), que podrían estar relacionados a la dieta de las aves. Entre estas, las especies con
mayor número de representantes (mayoritariamente pre-adultos) fueron Bulimulus bonariensis bonariensis y
Succinea meridionalis. Los nidos de Anumbius annumbi y Furnarius rufus de la provincia de Buenos Aires tuvieron el número más elevado de ejemplares de gasterópodos. Especímenes de gasterópodos de agua dulce (Heleobia
parchappii, Biomphalaria sp. y Drepanotrema sp.) constituyeron 13 % del total.
Palabras clave: Moluscos, gasterópodos acuáticos, gasterópodos terrestres, Pupisoma, aves, habitantes de nidos, dieta.
_____________
INTRODUCTION
The nests of birds constitute a microenvironment that provides organic material and shelter
for a diverse suite of invertebrates (insects, spiders, pseudoscorpions, and ticks), which inhabit
these nests in varying abundance (Di Iorio &
Turienzo, 2009, 2011; Turienzo & Di Iorio, 2008,
2010, 2011, 2014a). Nevertheless, data about the
occurrence of American gastropods in birds’ nests
are scarcely found in literature (Appendix 1).
The probable causes of the presence of snails
in bird’s nests were in part suggested by Judd
(1963) and Nolan (1959). Judd (1963) reported,
“most of the snails were in nests constructed in
flood debris or in trees and shrubs at the river’s
edge.” One species found in the nests is “among
the commonest snail in flood debris, another is
found among damp under leaves in densely shaded places, a third is found on low ground near
streams, and a fourth, “the snail found most
commonly in the nests, as well as being in nests
along the river, is also found climbing trees”.
Thus, in these cases, birds’ nests also serve as
an extension of the natural habitat of the species
already present on the branches and foliage.
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Revista del Museo Argentino de Ciencias Naturales, n. s. 17(1), 2015
Fig. 1. Distribution of gastropods in birds’ nests from Argentina.
According to Nolan (1959), Roscoe (1955) tells
of the discovery of aquatic snails on birds’ plumage. Ramsden (1914), McAtee (1914), and Paton
& Williamson (1943) refer to similar episodes involving terrestrial snails, i.e. that the snails are
involuntarily transported by the birds. Vagvolgyi
(1975) postulated that a species of petrel could
be responsible for the introduction of the micromolusk Nesopupa galapagensis Vagvolgyi,
1974 to the Galápagos Islands (Miquel & Herrera,
2014). The physiological and/or behavioral features of each species must be considered, e.g.,
the characteristics of the pedal mucus of species of Succinea, which is particularly adhesive,
could help the passive transport of this gastropod (Vagvolgyi, 1975). In recent years, it was
observed that operculate gastropods can survive
the passage through the digestive tract of birds
(Kawakami et al., 2008; van Leeuwen et al.,2012;
Wada et al.,2012; Rusiecki & Rusiecka, 2013).
There are several historical records of freshwater snails (Ampullariidae, Cochliopidae,
Planorbidae) as food items of some birds from
Argentina (Aravena, 1928, Zotta, 1932, 1934,
1936, 1940), as well as records of some unidentified fragments of a mollusk in the digestive tract of Coryphistera alaudina Burmeister,
1866 [Furnariidae] (Olrog, 1956). In the case
of Furnariidae birds, it was observed that prey
remains can be disregarded inside the nests, in
form of fragments (Turienzo & Di Iorio, 2008,
2010, 2014a), or in regurgitated pellets (Turienzo
& Di Iorio, 2014b).
This study presents the first records of ter-
Miquel et al.: Gastropod species found in birds’ nests
restrial gastropods found in avian nests from
Argentina, alive or dead, in Argentina. The purpose of this work is to present new information
about the existence of a relationship between
birds and continental mollusks, which could provide information about the spreading of gastropods by avian species.
MATERIALS AND METHODS
Extensive research on invertebrate communities in birds’ nests from Argentina was undertaken between 2005 and 2010, encompassing a total
of 695 nests belonging to 13 bird families from
14 provinces (Turienzo & Di Iorio, 2014b). Nest
identifications were made following the nest descriptions of De la Peña (1987, 2005) and Narosky
et al. (1983), and by the observation of the birds
following Narosky & Yzurieta (2003). Each nest
was entirely removed from the tree branches,
placed in a bag, and taken to the laboratory where
it was dissected. All invertebrates were manually
collected and preserved by P. Turienzo and O. Di
Iorio. The diet items of 11 species of Furnariidae
(included in the present work) were summarized
by Turienzo & Di Iorio (2014b).
Snails were identified by the senior author and
housed in the Invertebrate Division of the Museo
Argentino de Ciencias Naturales “Bernardino
Rivadavia”. Abbreviations used: D: diameter; H:
height; MACN-In: Invertebrate Collection, Museo
Argentino de Ciencias Naturales “Bernardino
Rivadavia”, Buenos Aires, Argentina.
RESULTS
The following birds’ nests from Argentina were
positive for mollusk findings inside them: Milvago
chimango Viellot, 1816 [Falconidae]; Anumbius
annumbi (Viellot, 1817); Asthenes dorbignyi
(Reichenbach, 1853); Furnarius rufus (Gmelin,
1788); Phacellodomus striaticollis Orbigny &
Lafresnaye, 1838; Schoeniophylax phryganophila
(Viellot, 1817); Coryphistera alaudina Burmeister,
1860; Pseudoseisura lophotes (Reichenbach, 1853)
[Furnariidae], the nests of this last species remodeled and occupied by Myiopsitta monachus catita
(Olrog, 1976) [Psittacidae]; Passer domesticus (L.,
1758) [Passeridae], outside and inside the nests of
F. rufus; Myiopsitta monachus catita Olrog, 1976
[Psittacidae]; Sicalis flaveola pelzelni Sclater,
1872 [Aves: Thraupidae], inside the nests of F. rufus; Turdus amaurochalinus Cabanis, 1850 [Aves:
Turdidae], and in one undetermined nest of an inquiline bird inside a nest of F. rufus (Table 1).
89
A total of 138 gastropods were found in 42
nests, representing 6.04 % of the whole sampled
nests (Turienzo & Di Iorio, 2014b), belonging
to 14 species in seven families of birds from six
Argentine provinces (Table 1). About 69 % of
the positive nests were of birds in the family
Furnariidae (n = 29), especially in 13 nests of A.
annumbi. The nests of F. rufus are closed domed
nests build with mud, which eventually serves as
nidification sites for other birds, such as S. f. pelzelni, P. domesticus and P. chalybea, where also
snails were found, as well as in nests of F. rufus
without inquiline birds (Table 1).
The snails were distributed across 11 species,
10 genera and 8 families. Out of this total, 7 species were soil-related, and 4 taxa were limnic species (Table 2). The average number of snails by
bird species was 6.66. However, Pupisoma latens
accounted for 58 live specimens in a single nest.
All the remaining gastropods were collected as
empty shells, with a low abundance (1.86 shells
by nest). Thirty percent of the specimens were
fragmented shells.
Cochliopidae
Heleobia parchappii (Orbigny, 1835)
(Fig. 2A)
Material examined. Buenos Aires: Chascomús,
11-VIII-2009, 3 exs. [MACN-In 38363], in nest of
A. annumbi # 1 on Celtis tala; Chascomús, 28-I2010, 8 exs. [MACN-In 38364], in nest of F. rufus
# 7 (+ Sicalis flaveola pelzelni), on Populus sp.,
1 ex. [MACN-In 38362], in nest of F. rufus (+
Sicalis flaveola pelzelni); Chascomús, 15-IX-2009,
1 ex. [MACN-In 38365], in nest of F. rufus # 1
+ Passer domesticus, on Celtis tala; Chascomús,
23-III-2010, 1 ex. [MACN-In 39097], in nest of
F. rufus # 9 + nest of Progne chalybea (Gmelin,
1789) [Hirundinidae] on Melia azedarach;
Ciudad Autónoma de Buenos Aires: Ciudad
Universitaria, 19-VIII-2008, 1 ex. [MACN-In
37508], in nest of F. rufus; Ciudad Universitaria,
28-VII-2008, 1 ex. [MACN-In 37509], in nest of T.
amaurochalinus on Celtis australis
Measurements of the illustrated specimen.
D: 4.0 x H: 1.5 mm, 5.5 whorls.
Distribution. Entre Ríos, Santa Fe, Buenos
Aires, La Pampa, Río Negro provinces (Gaillard
& Castellanos, 1977).
Remark. The analyzed specimens were adults,
ranging between 4 to 5 mm in length with seven
to eight whorls.
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Revista del Museo Argentino de Ciencias Naturales, n. s. 17(1), 2015
Table 1: Bird families species and numbers of nests positive for Gastropoda in Argentina. Abbreviations
of Argentinian provinces: BA, Buenos Aires (both province and Ciudad Autónoma); Cb, Córdoba;
Ch, Chaco; ER, Entre Ríos; LP, La Pampa; Sa, Salta.
Family
Bird species
Falconidae
Milvago chimango
Furnariidae
Anumbius annumbi
Furnariidae
Asthenes dorbignyi
Furnariidae
Coryphistera alaudina
Furnariidae
Furnarius rufus
Furnariidae
Phacellodomus sibilatrix
Furnariidae
Phacellodomus striaticollis
Furnariidae
Pseudoseisura lophotes (with M. monachus)
Furnariidae
Schoeniophylax phryganophila
Hirundinidae
Progne chalybea (inside F. rufus nest)
Passeridae
Passer domesticus (outside)
Passeridae
Passer domesticus (inside F. rufus nests)
Psittacidae
Myiopsitta monachus
Thraupidae
Sicalis flaveola pelzelni (inside F. rufus nests)
Turdidae
Turdus amaurochalinus
Undetermined
Inquiline bird (inside F. rufus nest)
Total
Sa
Ch
Cb
ER
1
LP
1
BA
Total
1
1
11
13
1
1
1
3
2
2
2
2
2
3
3
2
2
3
3
1
1
2
2
2
2
1
1
4
4
1
1
1
1
1
3
4
3
2
29
42
Planorbidae
Biomphalaria sp.
(Fig. 2B)
Succineidae
Succinea meridionalis Orbigny, 1846
(Fig. 2D)
Material examined. Entre Ríos: Crespo, 15-IX2009, 1 ex. [MACN-In 38366], in nest of P. domesticus, on Acacia caven; Buenos Aires: Vuelta de
Obligado, 27-IX-2008, 1 ex. [MACN-In 38368], in
nest of F. rufus + inquiline bird, on Broussonetia
papyrifera.
Measurements of the illustrated specimen.
D: 3.5 x H: 1.5 mm, 4.50 whorls.
Distribution. America and Africa (Rumi,
1991).
Remark. The analyzed specimens were juveniles.
Material examined. Córdoba: Mina Clavero,
14-VII-2009, 3 exs. [MACN-In 38376], in nest
of Pseudoseisura lophotes # 3 (remodeled by
Myiopsitta monachus) on Prosopis flexuosa;
Buenos Aires: Junín, 4 exs. [MACN-In 37462], in
nest of Passer domesticus; Estación Río Luján,
8-I-2009, 2 exs. [MACN-In 37540], in nest of A.
annumbi on Schinus sp.; Estación Río Luján,
30-X-2009, 3 exs. [MACN-In 38341], in nest of
A. annumbi on Schinus sp.; Estación Río Luján,
27-V-2009, 1 ex. [MACN-In 38342], in nest of A.
annumbi on Celtis tala; La Pampa: Santa Rosa,
7-II-2008, 2 exs. [MACN-In 38343], in one old
nest of A. annumbi occupied by inquilines on
Geoffroea decorticans.
Measurements of the illustrated specimen.
D: 7.0 x H: 3.5 mm, 3.25 whorls.
Distribution. Brazil, Paraguay, Uruguay;
Argentina: north and central areas to northern Patagonia (Castellanos & Landoni, 1995;
Simone, 2006).
Remarks: The average total length of the shells
Drepanotrema sp.
(Fig. 2C)
Material examined. Entre Ríos: Crespo, 26XII-2009, 1 ex. [MACN-In 38367], in nest of
Passer domesticus # 4 on Acacia caven.
Measurements of the illustrated specimen.
D: 4.5 x H: 4.0 mm, 5 whorls.
Distribution. South America (Rumi, 1991).
Miquel et al.: Gastropod species found in birds’ nests
91
1
8
TOTAL
Schoeniophylax phryganophila
Pseudoseisura lophotes
Phacellodomus sibilatrix
1
4
3
15
3
16
3
6
2
2
4
1
1
32
2
Lamellaxis gracilis
2
1
1
1
1
1
2
Pupisoma latens *
5
58
Zonitoides arboreus
TOTAL
13
2
Naesiotus deletangi
Paralaoma servilis
1
1
1
Pupoides paredesi
Bulimulus b. bonariensis
Phacellodomus striaticollis
11
Drepanotrema sp.
Succinea meridionalis
Passer domesticus
Myiopsitta monachus
Milvago chimango
Furnarius rufus + Sicalis sp.
Coryphistera alaudina
3
Biomphalaria sp.
Turdus amaurochalinus
Heleobia parchappii
Asthenes dorbignyi
Anumbius annumbi
Table 2. Number of gastropods specimens (mostly shells) found in bird’s nests in Argentina, shown
for each avian species. * The only species found alive in a nest is Pupisoma latens.
58
3
28
3
6
18
of this species collected from avian nests was 6.8
mm (pre-adults).
Pupillidae
Pupoides paredesii (Orbigny, 1835)
(Fig. 2E)
Material examined. Salta: La Poma, 27-XI2008, 3 exs. [MACN-In 37538], in nest of Asthenes
dorbignyi on Trichocereus atacamensis.
Measurements of the illustrated specimen.
D: 5.0 x H: 1.5 mm, 6.25 whorls.
Distribution. Ecuador, Perú, Bolivia, Chile;
Argentina: Jujuy (Hylton Scott, 1945; Fernández,
1973).
Subulinidae
Lamellaxis (Allopeas) gracilis (Hutton,
1834)
Material examined. La Pampa: Paraje La
Araña, 2-III-2008, 1 ex. ���������������������
[MACN-In 37463], broken, in nest of Myiopsitta monachus on Prosopis
caldenia.
Distribution. Worldwide, tropical and temperate regions, transported by the man. In
3
2
1
6
5
3
61
3
1
138
Argentina, Tucumán, Catamarca, Misiones,
Corrientes, Entre Ríos, La Pampa and Buenos
Aires provinces (Virgillito, 2012).
Vallonidae
Pupisoma latens Hylton Scott, 1960
(Fig. 2F-G)
Material examined. Córdoba: Mina Clavero,
22-I-2010, 58 exs. [MACN-In 38361], in nest
of Pseudoseisura lophotes # 3 (occupied by
Myiopsitta monachus) on Prosopis flexuosa.
Measurements of the illustrated specimen.
D: 1.0 x H: 1.0 mm, 2.5 whorls.
Distribution. Córdoba: Cabana (Hylton Scott,
1960; Fernández, 1973).
Remarks. The analyzed specimens ranged from
1.3 to 4.5 mm in size.This species was preliminarily considered to be conspecific with P. comicolense (Baker, 1928) by Hausdorf (2007), because
there are apparently intermediate specimens between the extreme forms of the latter. This taxonomic statement requires further research.
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Revista del Museo Argentino de Ciencias Naturales, n. s. 17(1), 2015
Bulimulidae
Bulimulus bonariensis bonariensis
(Rafinesque, 1833)
(Fig. 2H)
Material examined. Chaco: Route 90, Km
21, 3-XII-2008, 1 ex. [MACN-In 37539], in nest
of Coryphistera alaudina on Prosopis alba; El
Espinillo, 6-I-2010, 1 ex. [MACN-In 38354], in
nest of Phacellodomus sibilatrix # 4 (with three
nestlings), on Prosopis ruscifolia; Córdoba: Mina
Clavero, 14-VII-2009, 4 exs. [MACN-In 38357], in
nest of C. alaudina # 2 on Acacia atramentaria,
1 ex. [MACN-In 38352], in nest of Coryphistera
alaudina # 3, on Ulmus sp.; Entre Ríos: Crespo,
24-XII-2009, 1 ex. [MACN-In 38351], in nest of A.
annumbi, on Acacia caven; Buenos Aires: Campo
de Mayo, 3-XII-2005, 8 exs. [MACN-In 37177],
in nest of A. annumbi on Celtis tala: Campo de
Mayo, 27-VIII-2005, 1 ex. [MACN-In 37511],
in nest of A. annumbi on Celtis tala; Campo de
Mayo, 16-I-2010, 1 ex. [MACN-In 38349], in nest
of Schoeniophylax phryganophila on Celtis tala;
Campo de Mayo, 12-XII-2009, 2 exs. [MACN-In
38358], in nest of Milvago chimango; Vuelta de
Obligado, 27-IX-2008, 1 ex. [MACN-In 37522], in
nest of Phacellodomus striaticollis, on Celtis tala;
Estación Río Luján, 15-IX-2008, 1 ex. [MACN-In
37523], in nest of P. striaticollis; Estación Río
Luján, 21-IV-2009, 2 exs. [MACN-In 38344], in
nest of A. annumbi on Celtis tala; Estación Río
Luján, 30-IX-2009, 1 ex. [MACN-In 38345], in
nest of F. rufus (+ Sicalis flaveola pelzelni) on
Celtis tala; Estación Río Luján, 30-IX-2009, 1
ex. [MACN-In 38347], in nest of A. annumbi;
Estación Río Luján, 3-XII-2009, 1 ex. [MACNIn 38353], in nest of A. annumbi on Celtis tala;
Estación Río Luján, 27-V-2009, 1 ex. [MACN-In
38356], in nest of A. annumbi on Celtis tala;
Estación Río Luján, 31-III-2009, 1 ex. [MACN-In
38359], in nest of F. rufus # 1 (+ Sicalis flaveola
pelzelni); Estación Río Luján, 26-VI-2009, 1 ex.
[MACN-In 38360], in nest of A. annumbi # 2 on
Celtis tala; Zelaya, 25-VII-2009, 2 exs. [MACN-In
38346], in nest of Phacellodomus striaticollis #
1 on Celtis tala.
Measurements of the illustrated specimen.
D: 25.0 x H: 11.0 mm, 6 whorls.
Distribution. Uruguay. Chaco-pampean and
mesopotamic regions of Argentina (Miquel, 1991;
Miquel & Aguirre, 2011).
Remarks: Only five out of 32 specimens of this
species were adults or pre-adults (shell size between 15.5 and 19.0 mm and 6 whorls).
Naesiotus deletangi (Parodiz, 1946)
(Fig. 2I)
Material examined. Chaco: El Espinillo,
6-I-2010, 2 exs. [MACN-In 38355], in nest of
Phacellodomus sibilatrix.
Measurements of the illustrated specimen.
D: 5.5 x H: 3.0 mm, 5.50 whorls.
Remark. The analyzed specimens were juveniles.
Distribution. Northwest and central-west areas of
Argentina (Miquel, 1989; Miquel & Aguirre, 2011).
Punctidae
Paralaoma servilis (Shuttleworth, 1852)
(Fig. 2J-K)
Material examined. Buenos Aires: Junín, 26VIII-2008, 1 ex. [MACN-In 37510], in nest of
A. annumbi on Gleditsia triacanthos; Estación
Ingeniero Otamendi, 15-IX-2008, 1 ex. [MACN-In
37521], in nest of F. rufus on Celtis tala; Estación
Río Luján, 15-IX-2008, 1 ex. [MACN-In 37524],
in nest of P. striaticollis on Celtis tala; Campo
de Mayo, 16-I-2010, 2 exs. [MACN-In 38348], in
nest of S. phryganophila # 1-3 on Celtis tala.
Measurements of the illustrated specimen.
D: 2.5 x 1.5 mm, 4.5 whorls.
Distribution. Colombia; Brazil; Peru; Bolivia;
Chile; Argentina: Misiones, Tucumán, Formosa,
Santa Fe, Entre Ríos, Buenos Aires, Chubut;
Tierra del Fuego (Araya, 2015; Miquel & Barker,
2009; Virgillito & Miquel, 2013).
Zonitidae
Zonitoides arboreus (Say, 1817)
(Fig. 2L)
Material examined. Buenos Aires: Estación
Ingeniero Otamendi, 15-IX-2008, 3 exs. [MACNIn 37520], in nest of F. rufus on Celtis tala.
Measurements of the illustrated specimen.
D: 5.0 x H: 2.5 mm, 4.75 whorls.
Distribution. Europe, Israel, Kenia, South
Africa, Madagascar, Hong Kong, Japan, Hawaii,
North America, Australia; New Zealand, distributed by man (Pilsbry, 1946; Virgillito & Miquel,
2013); South America; Argentina: Jujuy, Salta,
Catamarca, Tucumán, Misiones, Corrientes,
Santiago del Estero, Córdoba, Entre Ríos; Buenos
Aires (Virgillito, 2012).
DISCUSSION
A comparison between the snail families
and the species found in birds’ nests from the
Miquel et al.: Gastropod species found in birds’ nests
93
Fig. 2. A. Heleobia parchappii (Orb., 1835). MACN-In 38364. Buenos Aires: Chascomús, in nest of Furnarius
rufus (Gmelin, 1788) + Sicalis sp., on Populus sp. B. Biomphalaria sp. MACN-In 38366. C. Drepanotrema sp.
MACN-In 38367. D. Succinea meridionalis Orb., 1846. MACN-In 38343. E. Pupoides paredesi (Orb.,1835).
MACN-In 37538. F-G. Pupisoma latens Hylton Scott, 1960. [MACN-In 38361]. H. Bulimulus b. bonariensis
(Rafinesque, 1833). MACN-In 38358. I. Naesiotus deletangi (Parodiz, 1946). MACN-In 38355. J-K. Paralaoma
servilis (Shuttleworth, 1852). MACN-In 38348. L. Zonitoides arboreus (Say, 1817). MACN-In 37520.
Northern and Southern Hemispheres shows
several coincidences: Pupillidae and species of
Pupoides were found in both regions, though
Pupoides albilabris (C. B. Adams) from Canada
was found alive, while P. paredesi was found dead;
Vallonidae were also found in both regions, though
the species found were from different genera
(Cionella Jeffreys, 1829, Gastrocopta Wollaston,
1878, Vallonia Risso, 1826, Novisuccinea Pilsbry,
1948, and others) and were, notably, found alive
in birds’ nests (Appendix 1).
Here only one species was found living in a
bird nest, a relatively large number of snails belonging to the native species Pupisoma latens.
This species is a micromollusk that lives on trees
in the native forests of Cabana (Córdoba province). It is small, corneous-colored and has a few
whorls (~ 3.5) (Hylton Scott, 1960). The current
record in Mina Clavero extends its natural distribution to the western area of Córdoba province
and confirms its presence in aerial habitats, e.g.,
nests of the Furnariidae Pseudoseisura lophotes as an extension of its natural habitat in the
branches and leaves of trees (Hylton Scott, 1960).
Another species in this genus (P. galapagorum
Pilsbry, 1934) was found living in Geospizzini
(finch) nests made of bryophytes and liverworts
in the Galapagos Islands.
As many of the specimens were found dead
(empty shells and/or fragments), they may be
part of the diet of the adult birds or nestlings.
This is an accidental transport, the most likely
form of transporting the aquatic and terrestrial
micromollusks cited here. Succinea meridionalis
and Bulimulus b. bonariensis, the two largest
snails registered, may be actively selected and
transported by the bird as a part of its diet, but
also the remaining species of snails found dead
in the birds’ nests can be regarded here as prey
items of the respective birds.
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Revista del Museo Argentino de Ciencias Naturales, n. s. 17(1), 2015
Among the dead gastropods found in the nests,
Bulimulus bonariensis bonariensis was the most
abundant shell, with 32 specimens (40 % of the
sample) in eight nests from Chaco and Córdoba.
The second most frequent species, Paralaoma
servilis, was found in four nests in Buenos Aires.
The less represented species were Drepanotrema
sp. (Entre Ríos), Lamellaxis gracilis (La Pampa)
and Pupoides paredesi (Salta), with only one
specimen each. Gastropod length was not uniform and there were fewer adults than juveniles.
Only 15 % of the specimens of Bulimulus b.
bonariensis were adults or pre-adults, while the
average total length of Succinea meridionalis
specimens was 6.8 mm (size of an adult usually is
over 10 mm). By the other side, only 13 % of the
species were freshwater snails (genera Heleobia
Stimpson, 1865, Biomphalaria Preston, 1910,
and Drepanotrema Crosse & Fischer, 1880), that
agree with the predation of aquatic organisms by
some of these terrestrial birds recorded in literature (Turienzo & Di Iorio 2014b).
CONCLUSIONS
The snail species recorded here from
Argentine bird’s nests can be grouped in two
classes: 1) those found living inside a nest, that
may be counted as inhabitants of this habitat,
and comprise a single species: Pupisoma latens,
and 2) those found dead inside bird’s nests, which
may be tentatively counted among the food items
of each bird: Heleobia parchappii, Biomphalaria
sp., Drepanotrema sp., Succinea meridionalis,
Pupoides paredesii, Lamellaxis (Allopeas) gracilis, Bulimulus b. bonariensis, Naesiotus deletangi, Paralaoma servilis, and Zonitoides arboreus.
Two plausible possibilities can be considered
regarding the presence of empty shells in the
nests. The first one is that these species were
passively transported by the birds to their nests,
where the snails subsequently died because of inadequate environmental conditions. The second
possibility is that bird’s nests function as a trap,
because their location inside the natural habitats of the snails allows the snails enter them
as a natural extension of their natural habitat,
but the snails die, as in the first case, due to the
complex structure of the nests (as in the cases
of Furnariidae oven nests and Psittacidae stick
nests in Argentina). Further sampling might
help answer these questions, deepening the comprehension of each species’ habitat and providing more information about live specimens inside birds’ nests.
ACKNOWLEDGEMENTS
The authors are grateful to F. Tricárico
(MACN), for the electronic micrographs. SEM and
PT belong to Consejo Nacional de Investigaciones
Científicas y Técnicas (CONICET).
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Appendix 1
Gastropods found in birds’ nests from
the Western Hemisphere mentioned in
literature
Arionidae
Arion hortensis (Férussac, 1819)
CANADA: Ontario: campus of the University
of Western Ontario, May 1960, one slug in
nest 62-2 (3 feet from the ground in a tangle of
leafless vines), identified by H. van der Schalie
(University of Michigan, Ann Arbor), from a total
of 32 examined nests of Cardinalis cardinalis
(Linnaeus, 1758) [= Richmondena cardinalis
(L.)] [Cardinalidae] (Judd, 1963).
Cionellidae
Cionella lubrica (Müller, 1774)
CANADA: Ontario: campus of the University
of Western Ontario, 11-V-1960, five snails in nest
65-2 (3 feet from the ground in flood debris),
identified by H. van der Schalie (University of
Michigan, Ann Arbor), from a total of 32 examined
nests of Cardinalis cardinalis (Linnaeus, 1758)
[= Richmondena cardinalis (L.)] [Cardinalidae]
(Judd, 1963).
Endodontidae
Anguispira alternata (Say, 1816)
CANADA: Ontario: campus of the University
of Western Ontario, 15/24-VII-1960, three snails
in nest 65-5 (10 feet from the ground in vines),
24-V/16-VI-1960, five snails in nest 66-1 (4 feet
from the ground in a Honeysuckle bush), 16V-1960, 3 snails in nest 613-1 (7 feet from the
ground in a red Cedar), identified by H. van der
Schalie (University of Michigan, Ann Arbor),
from a total of 32 examined nests of Cardinalis
cardinalis (Linnaeus, 1758) [= Richmondena
cardinalis (L.)] [Cardinalidae] (Judd, 1963).
Lymnaeidae
Pseudosuccinea columella (Say, 1817)
FRANCE: French Antilles: Guadeloupe:
one adult snail found in the Dadoud pond, in an
unidentified bird nest (Nicot et al., 2008).
Pupillidae
Gastrocopta armifera (Say, 1821)
UNITED STATES: Indiana: near Bloomington,
identified by J. E. P. Morrison, casual, one in
nest 1 of Dendroica discolor (Vieillot, 1809)
[Parulidae] (Nolan, 1955).
Pupoides albilabris (C. B. Adams, 1841)
UNITED STATES: Indiana: near Bloomington,
identified by J.P. E. Morrison, probably casual
(ordinarily terrestrial, a scavenger on plant and
animal material), one in nest 10 (15 inches high
in 2 ½-foot blackberry) of Dendroica discolor
(Vieillot, 1809) [Parulidae] (Nolan, 1959)
Note: According to Nolan (1959), “whether this
species and Gastrocopta armifera (previously
reported) were picked up by the warblers or
were carried to the nests as they clung to bits
of plant fiber, or whether they climbed up under
their own power, it is clear that this is another
instance in which a bird may become an agent in
dispersing small mollusks. Roscoe (1955) tells of
the discovery of aquatic snails on birds’ plumage,
and Ramsden (1914), McAtee (1914), and Paton
& Williamson (1943) refer to similar episodes
involving terrestrial snails”.
Succineidae
Novisuccinea ovalis (Say, 1817)
CANADA: Ontario: campus of the University
of Western Ontario, 18/20-V-1960, one snail in
nest 65-3 (3 feet from the ground in flood debris),
16-V-1960, 2 snails in nest 613-1 (7 feet from the
ground in a red Cedar), identified by H. van der
Schalie (University of Michigan, Ann Arbor),
from a total of 32 examined nests of Cardinalis
cardinalis (Linnaeus, 1758) [= Richmondena
cardinalis (L.)] [Cardinalidae] (Judd, 1963).
Vallonidae
Vallonia costata (Müller, 1774)
CANADA: Ontario: campus of the University
of Western Ontario, 11-V-1960, one snail in nest
65-2 (3 feet from the ground in flood debris),
identified by H. van der Schalie (University of
Michigan, Ann Arbor), from a total of 32 examined
nests of Cardinalis cardinalis (Linnaeus, 1758)
[= Richmondena cardinalis (L.)] [Cardinalidae]
(Judd, 1963).